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Annual Review of Genetics

Volume 52, 2018

Ribosome Hibernation

Abstract

Protein synthesis consumes a large fraction of available resources in the cell. When bacteria encounter unfavorable conditions and cease to grow, specialized mechanisms are in place to ensure the overall reduction of costly protein synthesis while maintaining a basal level of translation. A number of ribosome-associated factors are involved in this regulation; some confer an inactive, hibernating state of the ribosome in the form of 70S monomers (RaiA; this and the following are based on nomenclature) or 100S dimers (RMF and HPF homologs), and others inhibit translation at different stages in the translation cycle (RsfS, YqjD and paralogs, SRA, and EttA). Stationary phase cells therefore exhibit a complex array of different ribosome subpopulations that adjusts the translational capacity of the cell to the encountered conditions and ensures efficient reactivation of translation when conditions improve. Here, we review the current state of research regarding stationary phase-specific translation factors, in particular ribosome hibernation factors and other forms of translational regulation in response to stress conditions.

Keyword(s): 100S dimers, nutrient stress, ribosome, ribosome hibernation, stationary phase, translation
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2018-11-23
2024-04-26
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Literature Cited

  1. 1.  Agafonov DE, Kolb VA, Nazimov IV, Spirin AS 1999. A protein residing at the subunit interface of the bacterial ribosome. PNAS 96:12345–49
     [Google Scholar]
  2. 2.  Agafonov DE, Kolb VA, Spirin AS 2001. Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2:399–402
     [Google Scholar]
  3. 3.  Aiso T, Yoshida H, Wada A, Ohki R 2005. Modulation of mRNA stability participates in stationary-phase-specific expression of ribosome modulation factor. J. Bacteriol. 187:1951–58
     [Google Scholar]
  4. 4.  Akanuma G, Kazo Y, Tagami K, Hiraoka H, Yano K et al. 2016. Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis. Microbiology 162:448–58
     [Google Scholar]
  5. 5.  Akiyama T, Williamson KS, Schaefer R, Pratt S, Chang CB, Franklin MJ 2017. Resuscitation of Pseudomonas aeruginosa from dormancy requires hibernation promoting factor (PA4463) for ribosome preservation. PNAS 114:3204–209
     [Google Scholar]
  6. 6.  Ancona V, Li W, Zhao Y 2014. Alternative sigma factor RpoN and its modulation protein YhbH are indispensable for Erwinia amylovora virulence. Mol. Plant Pathol. 15:58–66
     [Google Scholar]
  7. 7.  Apirakaramwong A, Kashiwagi K, Raj VS, Sakata K, Kakinuma Y et al. 1999. Involvement of ppGpp, ribosome modulation factor, and stationary phase-specific sigma factor ςS in the decrease in cell viability caused by spermidine. Biochem. Biophys. Res. Commun. 264:643–47
     [Google Scholar]
  8. 8.  Arunasri K, Adil M, Khan PA, Shivaji S 2014. Global gene expression analysis of long-term stationary phase effects in E. coli K12 MG1655. PLOS ONE 9:e96701
     [Google Scholar]
  9. 9.  Basu A, Yap M-NF 2016. Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res 44:4881–93
     [Google Scholar]
  10. 10.  Basu A, Yap M-NF 2017. Disassembly of the Staphylococcus aureus hibernating 100S ribosome by an evolutionarily conserved GTPase. PNAS 114:E8165–73First evidence that an active mechanism is responsible for the dissociation of 100S in Staphylococcus aureus.
     [Google Scholar]
  11. 11.  Beckert B, Abdelshahid M, Schäfer H, Steinchen W, Arenz S et al. 2017. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J 36:2061–72One of four recent high-resolution cryo-electron microscopy structures of the long hibernation promoting factor (lHPF)–100S dimer.
     [Google Scholar]
  12. 11a.  Beckert B, Turk M, Czech A, Berninghausen O, Beckmann R et al. 2018. Structure of a hibernating 100S ribosome reveals an inactive conformation of the ribosomal protein S1. Nat. Microbiol 3:1115–21High-resolution cryo-electron microscopy structure of the hibernating Escherichia coli 70S and 100S ribosome.
     [Google Scholar]
  13. 12.  Bergkessel M, Basta DW, Newman DK 2016. The physiology of growth arrest: uniting molecular and environmental microbiology. Nat. Rev. Microbiol. 14:549–62
     [Google Scholar]
  14. 13.  Bieri P, Leibundgut M, Saurer M, Boehringer D, Ban N 2017. The complete structure of the chloroplast 70S ribosome in complex with translation factor pY. EMBO J 36:475–86
     [Google Scholar]
  15. 14.  Boël G, Smith PC, Ning W, Englander MT, Chen B et al. 2014. The ABC-F protein EttA gates ribosome entry into the translation elongation cycle. Nat. Struct. Mol. Biol. 21:143–51
     [Google Scholar]
  16. 15.  Boerema AP, Aibara S, Paul B, Tobiasson V, Kimanius D et al. 2018. Structure of the chloroplast ribosome with chl-RRF and hibernation-promoting factor. Nat. Plants 4:212–17
     [Google Scholar]
  17. 16.  Bonocora RP, Smith C, Lapierre P, Wade JT 2015. Genome-scale mapping of Escherichia coli σ54 reveals widespread, conserved intragenic binding. PLOS Genet 11:e1005552
     [Google Scholar]
  18. 17.  Breüner A, Frees D, Varmanen P, Boguta AM, Hammer K et al. 2016. Ribosomal dimerization factor YfiA is the major protein synthesized after abrupt glucose depletion in Lactococcus lactis. Microbiology 162:1829–39
     [Google Scholar]
  19. 18.  Bubunenko M, Baker T, Court DL 2007. Essentiality of ribosomal and transcription antitermination proteins analyzed by systematic gene replacement in Escherichia coli. J. Bacteriol 189:2844–53
     [Google Scholar]
  20. 19.  Bubunenko MG, Subramanian AR 1994. Recognition of novel and divergent higher plant chloroplast ribosomal proteins by Escherichia coli ribosome during in vivo assembly. J. Biol. Chem. 269:18223–31
     [Google Scholar]
  21. 20.  Carlson PE, Carroll JA, O'Dee DM, Nau GJ 2007. Modulation of virulence factors in Francisella tularensis determines human macrophage responses. Microbial. Pathog. 42:204–14
     [Google Scholar]
  22. 21.  Chen B, Boël G, Hashem Y, Ning W, Fei J et al. 2014. EttA regulates translation by binding the ribosomal E site and restricting ribosome-tRNA dynamics. Nat. Struct. Mol. Biol. 21:152–59
     [Google Scholar]
  23. 22.  DeLisa MP, Wu C-F, Wang L, Valdes JJ, Bentley WE 2001. DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J. Bacteriol 183:5239–47
     [Google Scholar]
  24. 23.  Di Pietro F, Brandi A, Dzeladini N, Fabbretti A, Carzaniga T et al. 2013. Role of the ribosome-associated protein PY in the cold-shock response of Escherichia coli. Microbiologyopen 2:293–307
     [Google Scholar]
  25. 24.  Drzewiecki K, Eymann C, Mittenhuber G, Hecker M 1998. The yvyD gene of Bacillus subtilis is under dual control of σB and σH. J. Bacteriol. 180:6674–80
     [Google Scholar]
  26. 25.  Durfee T, Hansen AM, Zhi H, Blattner FR, Jin DJ 2008. Transcription profiling of the stringent response in Escherichia coli. J. Bacteriol 190:1084–96
     [Google Scholar]
  27. 26.  El-Sharoud WM, Niven GW 2005. The activity of ribosome modulation factor during growth of Escherichia coli under acidic conditions. Arch. Microbiol. 184:18–24
     [Google Scholar]
  28. 27.  El-Sharoud WM, Niven GW 2007. The influence of ribosome modulation factor on the survival of stationary-phase Escherichia coli during acid stress. Microbiology 153:247–53
     [Google Scholar]
  29. 28.  Fazzino L, Tilly K, Dulebohn DP, Rosa PA 2015. Long-term survival of Borrelia burgdorferi lacking the Hibernation Promotion Factor homolog in the unfed tick vector. Infect. Immun. 83:4800–10
     [Google Scholar]
  30. 29.  Franken LE, Oostergetel GT, Pijning T, Puri P, Arkhipova V et al. 2017. A general mechanism of ribosome dimerization revealed by single-particle cryo-electron microscopy. Nat. Commun. 8:722One of four recent high-resolution cryo-electron microscopy structures of the long hibernation promoting factor (lHPF)–100S dimer.
     [Google Scholar]
  31. 30.  Fukuchi J-i, Kashiwagi K, Yamagishi M, Ishihama A, Igarashi K 1995. Decrease in cell viability due to the accumulation of spermidine in spermidine acetyltransferase-deficient mutant of Escherichia coli. J. Biol. Chem 270:18831–35
     [Google Scholar]
  32. 31.  Galmozzi CV, Florencio FJ, Muro-Pastor MI 2016. The cyanobacterial ribosomal-associated protein LrtA is involved in post-stress survival in Synechocystis sp. PCC 6803. PLOS ONE 11:e0159346
     [Google Scholar]
  33. 32.  Gao Y-G, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326:694–99
     [Google Scholar]
  34. 33.  Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J. Biol. Chem. 275:5668–74
     [Google Scholar]
  35. 34.  Gefen O, Fridman O, Ronin I, Balaban NQ 2014. Direct observation of single stationary-phase bacteria reveals a surprisingly long period of constant protein production activity. PNAS 111:556–61
     [Google Scholar]
  36. 35.  Goldstein A, Goldstein DB, Brown BJ, Chou S-C 1959. Amino acid starvation in an Escherichia coli auxotroph: I. Effects on protein and nucleic acid synthesis and on cell division. Biochim. Biophys. Acta 36:163–72
     [Google Scholar]
  37. 36.  Goujon M, McWilliam H, Li W, Valentin F, Squizzato S et al. 2010. A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Res 38:W695–99
     [Google Scholar]
  38. 37.  Graf M, Arenz S, Huter P, Donhofer A, Novacek J, Wilson DN 2017. Cryo-EM structure of the spinach chloroplast ribosome reveals the location of plastid-specific ribosomal proteins and extensions. Nucleic Acids Res 45:2887–96
     [Google Scholar]
  39. 38.  Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M 2004. “Sleeping Beauty”: quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev 68:187–206
     [Google Scholar]
  40. 39.  Guo Y, Liu X, Li B, Yao J, Wood TK, Wang X 2017. Tail-anchored inner membrane protein ElaB increases resistance to stress while reducing persistence in Escherichia coli. J. Bacteriol 199:e00057–17
     [Google Scholar]
  41. 40.  Hall CE, Slayter HS 1959. Electron microscopy of ribonucleoprotein particles from E. coli.J. Mol. Biol 1:329–32One of several seminal papers describing the components of the translation machinery, including 100S dimers.
     [Google Scholar]
  42. 41.  Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K 2015. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat. Rev. Microbiol. 13:298–309
     [Google Scholar]
  43. 42.  Häuser R, Pech M, Kijek J, Yamamoto H, Titz B et al. 2012. RsfA (YbeB) proteins are conserved ribosomal silencing factors. PLOS Genet 8:e1002815
     [Google Scholar]
  44. 43.  Hood RD, Higgins SA, Flamholz A, Nichols RJ, Savage DF 2016. The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus. PNAS 113:E4867–76
     [Google Scholar]
  45. 44.  Hussain T, Llácer JL, Wimberly BT, Kieft JS, Ramakrishnan V Large-scale movements of IF3 and tRNA during bacterial translation initiation. Cell 167:133–44.e13
     [Google Scholar]
  46. 45.  Igarashi K, Kashiwagi K 2010. Modulation of cellular function by polyamines. Int. J. Biochem. Cell Biol. 42:39–51
     [Google Scholar]
  47. 46.  Izutsu K, Wada A, Wada C 2001. Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp. Genes Cells 6:665–76
     [Google Scholar]
  48. 47.  Izutsu K, Wada C, Komine Y, Sako T, Ueguchi C et al. 2001. Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase. J. Bacteriol. 183:2765–73
     [Google Scholar]
  49. 48.  Jones DH, Christopher F, Franklin H, Thomas CM 1994. Molecular analysis of the operon which encodes the RNA polymerase sigma factor σ54 of Escherichia coli. Microbiology 140:1035–43
     [Google Scholar]
  50. 49.  Kato T, Yoshida H, Miyata T, Maki Y, Wada A, Namba K 2010. Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy. Structure 18:719–24Describes cryo-electron microscopy structure of the Escherichia coli 100S dimer.
     [Google Scholar]
  51. 50.  Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–49
     [Google Scholar]
  52. 51.  Khusainov I, Vicens Q, Ayupov R, Usachev K, Myasnikov A et al. 2017. Structures and dynamics of hibernating ribosomes from Staphylococcus aureus mediated by intermolecular interactions of HPF. EMBO J 36:2073–87One of four recent high-resolution cryo-electron microscopy structures of the long hibernation promoting factor (lHPF)–100S dimer.
     [Google Scholar]
  53. 52.  Kline BC, McKay SL, Tang WW, Portnoy DA 2015. The Listeria monocytogenes hibernation-promoting factor is required for the formation of 100S ribosomes, optimal fitness, and pathogenesis. J. Bacteriol. 197:581–91
     [Google Scholar]
  54. 53.  Kolter R, Siegele DA, Tormo A 1993. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47:855–74
     [Google Scholar]
  55. 54.  Krokowski D, Gaccioli F, Majumder M, Mullins MR, Yuan CL et al. 2011. Characterization of hibernating ribosomes in mammalian cells. Cell Cycle 10:2691–702
     [Google Scholar]
  56. 55.  Landini P, Egli T, Wolf J, Lacour S 2014. sigmaS, a major player in the response to environmental stresses in Escherichia coli: role, regulation and mechanisms of promoter recognition. Environ. Microbiol. Rep. 6:1–13
     [Google Scholar]
  57. 56.  Lange R, Hengge-Aronis R 1991. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor σS. J. Bacteriol. 173:4474–81
     [Google Scholar]
  58. 57.  Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–48
     [Google Scholar]
  59. 58.  Li X, Sun Q, Jiang C, Yang K, Hung LW et al. 2015. Structure of ribosomal silencing factor bound to Mycobacterium tuberculosis ribosome. Structure 23:1858–65
     [Google Scholar]
  60. 58a.  Li Y, Sharma MR, Koripella RK, Yang Y, Kaushal PS et al. 2018. Zinc depletion induces ribosome hibernation in mycobacteria. PNAS 115:8191–96
     [Google Scholar]
  61. 59.  Liu K, Bittner AN, Wang JD 2015. Diversity in (p)ppGpp metabolism and effectors. Curr. Opin. Microbiol. 24:72–79
     [Google Scholar]
  62. 60.  Maki Y, Yoshida H, Wada A 2000. Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells 5:965–74
     [Google Scholar]
  63. 61.  Matamouros S, Hayden HS, Hager KR, Brittnacher MJ, Lachance K et al. 2018. Adaptation of commensal proliferating Escherichia coli to the intestinal tract of young children with cystic fibrosis. PNAS 115:1605–10
     [Google Scholar]
  64. 62.  Matzov D, Aibara S, Basu A, Zimmerman E, Bashan A et al. 2017. The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat. Commun 8:723One of four recent high-resolution cryo-electron microscopy structures of the long hibernation promoting factor (lHPF)–100S dimer.
     [Google Scholar]
  65. 63.  McCarthy BJ 1960. Variations in bacterial ribosomes. Biochim. Biophys. Acta 39:563–64One of several seminal papers describing the components of the translation machinery, including 100S dimers.
     [Google Scholar]
  66. 64.  McKay SL, Portnoy DA 2015. Ribosome hibernation facilitates tolerance of stationary-phase bacteria to aminoglycosides. Antimicrob. Agents Chemother. 59:6992–99
     [Google Scholar]
  67. 65.  Merrick MJ, Coppard JR 1989. Mutations in genes downstream of the rpoN gene (encoding σ54) of Klebsiella pneumoniae affect expression from σ54-dependent promoters. Mol. Microbiol. 3:1765–75
     [Google Scholar]
  68. 66.  Moen B, Janbu AO, Langsrud S, Langsrud O, Hobman JL et al. 2009. Global responses of Escherichia coli to adverse conditions determined by microarrays and FT-IR spectroscopy. Can. J. Microbiol. 55:714–28
     [Google Scholar]
  69. 67.  Monod J 1949. The growth of bacterial cultures. Annu. Rev. Microbiol. 3:371–94
     [Google Scholar]
  70. 68.  Navarro Llorens JM, Tormo A, Martínez-García E 2010. Stationary phase in gram-negative bacteria. FEMS Microbiol. Rev. 34:476–95
     [Google Scholar]
  71. 69.  Niven GW 2004. Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerisation. Arch. Microbiol. 182:60–66
     [Google Scholar]
  72. 70.  Deleted in proof
  73. 71.  Oosthuizen MC, Steyn B, Theron J, Cosette P, Lindsay D et al. 2002. Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl. Environ. Microbiol. 68:2770–80
     [Google Scholar]
  74. 72.  Ortiz JO, Brandt F, Matias VR, Sennels L, Rappsilber J et al. 2010. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J. Cell Biol. 190:613–21In situ evidence for 100S dimers in intact cells using cryo-electron tomography.
     [Google Scholar]
  75. 73.  Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605–12
     [Google Scholar]
  76. 74.  Piir K, Paier A, Liiv A, Tenson T, Maivali U 2011. Ribosome degradation in growing bacteria. EMBO Rep 12:458–62
     [Google Scholar]
  77. 75.  Polikanov YS, Blaha GM, Steitz TA 2012. How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 336:915–18High-resolution crystal structure of the Thermus thermophilus ribosome in complex with the Escherichia coli hibernation factors.
     [Google Scholar]
  78. 76.  Potrykus K, Cashel M 2008. (p)ppGpp: still magical?. Annu. Rev. Microbiol. 62:35–51
     [Google Scholar]
  79. 77.  Pulk A, Liiv A, Peil L, Maiväli Ü, Nierhaus K, Remme J 2010. Ribosome reactivation by replacement of damaged proteins. Mol. Microbiol. 75:801–14
     [Google Scholar]
  80. 78.  Puri P, Eckhardt TH, Franken LE, Fusetti F, Stuart MCA et al. 2014. Lactococcus lactisYfiA is necessary and sufficient for ribosome dimerization. Mol. Microbiol. 91:394–407
     [Google Scholar]
  81. 79.  Raivio TL, Leblanc SKD, Price NL 2013. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J. Bacteriol. 195:2755–67
     [Google Scholar]
  82. 80.  Rak A, Kalinin A, Shcherbakov D, Bayer P 2002. Solution structure of the ribosome-associated cold shock response protein Yfia of Escherichia coli. Biochem. Biophys. Res. Commun 299:710–14
     [Google Scholar]
  83. 81.  Ramakrishnan V 2002. Ribosome structure and the mechanism of translation. Cell 108:557–72
     [Google Scholar]
  84. 82.  Sabharwal D, Song T, Papenfort K, Wai SN 2015. The VrrA sRNA controls a stationary phase survival factor Vrp of Vibrio cholerae. RNA Biol 12:186–96Describes the first small RNA reported to be involved in the regulation of hibernation factor expression.
     [Google Scholar]
  85. 83.  Samartzidou H, Widger WR 1998. Transcriptional and posttranscriptional control of mRNA from lrtA, a light-repressed transcript in Synechococcus sp. PCC 7002. Plant Physiol 117:225–34
     [Google Scholar]
  86. 84.  Samuel Raj V, Füll C, Yoshida M, Sakata K, Kashiwagi K et al. 2002. Decrease in cell viability in an RMF, σ38, and OmpC triple mutant of Escherichia coli. Biochem. Biophys. Res. Commun 299:252–57
     [Google Scholar]
  87. 85.  Sato A, Watanabe T, Maki Y, Ueta M, Yoshida H et al. 2009. Solution structure of the E. coli ribosome hibernation promoting factor HPF: implications for the relationship between structure and function. Biochem. Biophys. Res. Commun. 389:580–85
     [Google Scholar]
  88. 86.  Schmeing TM, Ramakrishnan V 2009. What recent ribosome structures have revealed about the mechanism of translation. Nature 461:1234–42
     [Google Scholar]
  89. 87.  Schrödinger LLC 2015. The PyMOL Molecular Graphics System, Version 2.0.6. http://pymol.org/
  90. 88.  Sharma MR, Dönhöfer A, Barat C, Marquez V, Datta PP et al. 2010. PSRP1 is not a ribosomal protein, but a ribosome-binding factor that is recycled by the ribosome-recycling factor (RRF) and elongation factor G (EF-G). J. Biol. Chem. 285:4006–14
     [Google Scholar]
  91. 89.  Sharma MR, Wilson DN, Datta PP, Barat C, Schluenzen F et al. 2007. Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. PNAS 104:19315–20
     [Google Scholar]
  92. 90.  Shcherbakova K, Nakayama H, Shimamoto N 2015. Role of 100S ribosomes in bacterial decay period. Genes Cells 20:789–801
     [Google Scholar]
  93. 91.  Shimada T, Makinoshima H, Ogawa Y, Miki T, Maeda M, Ishihama A 2004. Classification and strength measurement of stationary-phase promoters by use of a newly developed promoter cloning vector. J. Bacteriol. 186:7112–22
     [Google Scholar]
  94. 92.  Shimada T, Yoshida H, Ishihama A 2013. Involvement of cyclic AMP receptor protein in regulation of the rmf gene encoding the ribosome modulation factor in Escherichia coli. J. Bacteriol 195:2212–19
     [Google Scholar]
  95. 93.  Starosta AL, Lassak J, Jung K, Wilson DN 2014. The bacterial translation stress response. FEMS Microbiol. Rev. 38:1172–201
     [Google Scholar]
  96. 94.  Steitz TA 2008. A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 9:242–53
     [Google Scholar]
  97. 95.  Storz G, Hengge R, eds. 2011. Bacterial Stress Responses Washington, DC: Am. Soc. Microbiol. , 2nd ed..
  98. 96.  Sulthana S, Basturea GN, Deutscher MP 2016. Elucidation of pathways of ribosomal RNA degradation: an essential role for RNase E. RNA 22:1163–71
     [Google Scholar]
  99. 97.  Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S et al. 2012. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp0 mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen 1:115–34
     [Google Scholar]
  100. 98.  Tan X, Varughese M, Widger WR 1994. A light-repressed transcript found in Synechococcus PCC 7002 is similar to a chloroplast-specific small subunit ribosomal protein and to a transcription modulator protein associated with sigma 54. J. Biol. Chem. 269:20905–12
     [Google Scholar]
  101. 99.  Terui Y, Tabei Y, Akiyama M, Higashi K, Tomitori H et al. 2010. Ribosome modulation factor, an important protein for cell viability encoded by the polyamine modulon. J. Biol. Chem. 285:28698–707
     [Google Scholar]
  102. 100.  Tissières A, Watson JD 1958. Ribonucleoprotein particles from Escherichia coli. Nature 182:778–80One of several seminal papers describing the components of the translation machinery, including 100S dimers.
     [Google Scholar]
  103. 101.  Tkachenko AG, Kashevarova NM, Karavaeva EA, Shumkov MS 2014. Putrescine controls the formation of Escherichia coli persister cells tolerant to aminoglycoside netilmicin. FEMS Microbiol. Lett. 361:25–33
     [Google Scholar]
  104. 102.  Tkachenko AG, Kashevarova NM, Tyuleneva EA, Shumkov MS 2017. Stationary-phase genes upregulated by polyamines are responsible for the formation of Escherichia coli persister cells tolerant to netilmicin. FEMS Microbiol. Lett. 364:fnx084
     [Google Scholar]
  105. 103.  Traxler MF, Summers SM, Nguyen HT, Zacharia VM, Hightower GA et al. 2008. The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol. Microbiol 68:1128–48
     [Google Scholar]
  106. 104.  Ueta M, Ohniwa RL, Yoshida H, Maki Y, Wada C, Wada A 2008. Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli. J. Biochem 143:425–33
     [Google Scholar]
  107. 105.  Ueta M, Wada C, Bessho Y, Maeda M, Wada A 2017. Ribosomal protein L31 in Escherichia coli contributes to ribosome subunit association and translation, whereas short L31 cleaved by protease 7 reduces both activities. Genes Cells 22:452–71
     [Google Scholar]
  108. 106.  Ueta M, Wada C, Daifuku T, Sako Y, Bessho Y et al. 2013. Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells 18:554–74Describes two distinct forms of 100S dimers that differ in structure, stability, and patterns of formation.
     [Google Scholar]
  109. 107.  Ueta M, Wada C, Wada A 2010. Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog SaHPF. Genes Cells 15:43–58
     [Google Scholar]
  110. 108.  Ueta M, Yoshida H, Wada C, Baba T, Mori H, Wada A 2005. Ribosome binding proteins YhbH and YfiA have opposite functions during 100S formation in the stationary phase of Escherichia coli. Genes Cells 10:1103–12First insight into the distinct functions of Escherichia coli hibernation promoting factor (HPF) and ribosome-associated inhibitor A (RaiA).
     [Google Scholar]
  111. 109.  Vila-Sanjurjo A, Schuwirth B-S, Hau CW, Cate JHD 2004. Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol. 11:1054–59
     [Google Scholar]
  112. 110.  Voorhees RM, Weixlbaumer A, Loakes D, Kelley AC, Ramakrishnan V 2009. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16:528–33
     [Google Scholar]
  113. 111.  Wada A 1986. Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. II. Characterization of four new proteins. J. Biochem. 100:1595–605
     [Google Scholar]
  114. 112.  Wada A 1998. Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells 3:203–8
     [Google Scholar]
  115. 113.  Wada A, Igarashi K, Yoshimura S, Aimoto S, Ishihama A 1995. Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli. Biochem. Biophys. Res. Commun 214:410–17
     [Google Scholar]
  116. 114.  Wada A, Mikkola R, Kurland CG, Ishihama A 2000. Growth phase-coupled changes of the ribosome profile in natural isolates and laboratory strains of Escherichia coli. J. Bacteriol 182:2893–99
     [Google Scholar]
  117. 115.  Wada A, Yamazaki Y, Fujita N, Ishihama A 1990. Structure and probable genetic location of a “ribosome modulation factor” associated with 100S ribosomes in stationary-phase Escherichia coli cells. PNAS 87:2657–61Identification of ribosome modulation factor (RMF) as the putative factor involved in the formation of 100S dimers.
     [Google Scholar]
  118. 116.  Williamson KS, Richards LA, Perez-Osorio AC, Pitts B, McInnerney K et al. 2012. Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J. Bacteriol. 194:2062–73
     [Google Scholar]
  119. 117.  Wilson DN 2013. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat. Rev. Microbiol. 12:35–48
     [Google Scholar]
  120. 118.  Yamagishi M, Matsushima H, Wada A, Sakagami M, Fujita N, Ishihama A 1993. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase-and growth rate-dependent control. EMBO J 12:625–30
     [Google Scholar]
  121. 119.  Yamaguchi K, Subramanian AR 2000. The plastid ribosomal proteins: identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275:28466–82
     [Google Scholar]
  122. 120.  Yamaguchi K, von Knoblauch K, Subramanian AR 2000. The plastid ribosomal proteins: identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275:28455–65
     [Google Scholar]
  123. 121.  Ye K, Serganov A, Hu W, Garber M, Patel DJ 2002. Ribosome-associated factor Y adopts a fold resembling a double-stranded RNA binding domain scaffold. Eur. J. Biochem. 269:5182–91
     [Google Scholar]
  124. 122.  Yoshida H, Maki Y, Furuike S, Sakai A, Ueta M, Wada A 2012. YqjD is an inner membrane protein associated with stationary-phase ribosomes in Escherichia coli. J. Bacteriol 194:4178–83
     [Google Scholar]
  125. 123.  Yoshida H, Maki Y, Kato H, Fujisawa H, Izutsu K et al. 2002. The ribosome modulation factor (RMF) binding site on the 100S ribosome of Escherichia coli. J. Biochem 132:983–89
     [Google Scholar]
  126. 124.  Yoshida H, Ueta M, Maki Y, Sakai A, Wada A 2009. Activities of Escherichia coli ribosomes in IF3 and RMF change to prepare 100S ribosome formation on entering the stationary growth phase. Genes Cells 14:271–80
     [Google Scholar]
  127. 125.  Yoshida H, Wada A 2014. The 100S ribosome: ribosomal hibernation induced by stress. WIREs RNA 5:723–32
     [Google Scholar]
  128. 126.  Yoshida H, Yamamoto H, Uchiumi T, Wada A 2004. RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel. Genes Cells 9:271–78
     [Google Scholar]
  129. 127.  Yusupova G, Jenner L, Rees B, Moras D, Yusupov M 2006. Structural basis for messenger RNA movement on the ribosome. Nature 444:391–94
     [Google Scholar]
  130. 128.  Zundel MA, Basturea GN, Deutscher MP 2009. Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15:977–83
     [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035130
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Ribosome Hibernation
Annual Review of Genetics 52, 321 (2018); https://doi.org/10.1146/annurev-genet-120215-035130
/content/journals/10.1146/annurev-genet-120215-035130
/content/journals/10.1146/annurev-genet-120215-035130
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